Basolateral amygdala lesions block the disruptive effects of long-term adrenalectomy on spatial memory

Neuroscience

Volumn 84, Issue 2, 1998, Pages 453-465

  Roozendaal, B ^a   Sapolsky, R M ^b   McGaugh, J L ^a,c  

^a Ctr Neurbio of Lrng and Memory   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Corticosterone; Dentate gyrus neuronal degeneration; Glucocorticoid receptor; Hippocampus; Water maze

Indexed keywords

CORTICOSTERONE; GLUCOCORTICOID RECEPTOR; HORMONE; N METHYL DEXTRO ASPARTIC ACID; WATER;

ADRENALECTOMY; AMNESIA; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPUS; LEARNING; MALE; MAZE TEST; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; RADIOIMMUNOASSAY; RAT; SPATIAL MEMORY;

ADRENALECTOMY; AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; CORTICOSTERONE; DENTATE GYRUS; MALE; MAZE LEARNING; MEMORY; N-METHYLASPARTATE; NERVE DEGENERATION; RATS; RATS, SPRAGUE-DAWLEY; SPACE PERCEPTION; WEIGHT GAIN;

EID: 0031914007     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00538-1     Document Type: Article

References (62)

1. Cabib S., Castellano C., Patacchioli F. R., Cigliana G., Angelucci L., Puglisi-Allegra S. Opposite strain-dependent effects of post-training corticosterone in a passive avoidance task in mice: Role of dopamine. Brain Res. 729:1996;110-118.
2. Cahill L., Babinsky R., Markowitsch H. J., McGaugh J. L. The amygdala and emotional memory. Nature. 337:1995;295-296.
3. Cahill L., Haier R. J., Fallon J., Alkire M. T., Tang C., Keator D., Wu J., McGaugh J. L. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc. natn. Acad. Sci. U.S.A. 93:1996;8016-8021.
4. Cahill L., McGaugh J. L. Amygdaloid complex lesions differentially affect retention of tasks using appetitive and aversive reinforcement. Behav. Neurosci. 104:1990;532-543.
5. Conrad C. D., Roy E. J. Selective loss of hippocampal granule cells following adrenalectomy: Implications for spatial memory. J. Neurosci. 13:1993;2582-2590.
6. Conrad C. D., Roy E. J. Dentate gyrus destruction and spatial learning impairment after corticosteroid removal in young and middle-aged rats. Hippocampus. 5:1995;1-15.
7. de Kloet E. R., de Kock S., Schild V., Veldhuis H. D. Antiglucocorticoid RU 38486 attenuates retention of a behavior and disinhibits the hypothalamic-pituitary-adrenal axis at different sites. Neuroendocrinology. 47:1988;109-115.
8. deOlmos J., Alheid G. F. and Beltramino C. A. (1985) Amygdala. In The Rat Nervous System: Vol. 1, Forebrain and Midbrain (ed. Paxinos G.), pp. 223-334. Academic Press, New York.
9. Diamond D. M., Bennett M. C., Engström D. A., Fleshner M., Rose G. M. Adrenalectomy reduces the threshold for hippocampal primed burst potentiation in the anesthetized rat. Brain Res. 492:1989;356-360.
10. Diamond D. M., Bennett M. C., Fleshner M., Rose G. M. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus. 2:1992;421-426.
11. Emerich D. F., Walsh T. J. Cholinergic cell loss and cognitive impairments following intraventricular or intradentate injection of colchicine. Brain Res. 517:1990;157-167.
12. Gould E., Woolley C. S., McEwen B. S. Short-term glucocorticoid manipulations affect neuronal morphology and survival in the adult dentate gyrus. Neuroscience. 37:1990;367-375.
13. Gwosdon-Cohen A., Chen C., Besch E. Radioimmunoassay of serum corticosterone in rats. Proc. Soc. exp. Biol. 170:1982;29-39.
14. Honkaniemi J., Pelto-Huikko M., Rechardt L., Isola J., Lammi A., Fuxe K., Gustafsson J. Å., Wikström A.-C., Hökfelt T. Colocalization of peptide and glucocorticoid receptor immunoreactivities in rat central amygdaloid nucleus. Neuroendocrinology. 55:1992;451-459.
15. Ikegaya Y., Saito H., Abe K. Attenuated hippocampal long-term potentiation in basolateral amygdala-lesioned rats. Brain Res. 656:1994;157-174.
16. Ikegaya Y., Saito H., Abe K. Requirement of basolateral amygdala neuron activity for the induction of long-term potentiation in the dentate gyrus in vivo. Brain Res. 671:1995;351-354.
17. Islam A., Henriksson B., Mohammed A., Winblad B., Adem A. Behavioral deficits in adult rats following long-term adrenalectomy. Neurosci. Lett. 194:1995;49-52.
18. Jaarsma D., Postema F., Korf J. Time course and distribution of neuronal degeneration in the dentate gyrus of rat after adrenalectomy: A silver impregnation study. Hippocampus. 2:1992;143-150.
19. Joëls M., de Kloet E. R. Control of neuronal excitability by corticosteroid hormones. Trends Neurosci. 15:1992;25-30.
20. Kelley A. E., Domesick V. B., Nauta W. J. The amygdalostriatal projection in the rat: An anatomical study by anterograde and retrograde tracing methods. Neuroscience. 7:1982;615-630.
21. Kesner R. P. (1992) Learning and memory in rats with an emphasis on the role of the amygdala. In The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction (ed. Aggleton J. P.), pp. 370-399. Wiley-Liss, New York.
22. Korte S. M., de Kloet E. R., Buwalda B., Bouman S. D., Bohus B. Antisense to the glucocorticoid receptor in the hippocampal dentate gyrus reduces immobility in forced swim task. Eur. J. Pharmac. 301:1996;19-25.
23. Liang K. C., Hu S.-J., Chang S. C. Formation and retrieval of inhibitory avoidance memory: Differential roles of glutamate receptors in the amygdala and medial prefrontal cortex. Chin. J. Physiol. 39:1996;155-166.
24. Maren S., Fanselow M. S. Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo. J. Neurosci. 15:1995;7548-7564.
25. McEwen B. S., Weiss J. M., Schwartz L. S. Selective retention of corticosterone by limbic structures in the rat brain. Nature. 220:1968;911-912.
26. McGaugh J. L., Cahill L., Roozendaal B. Involvement of the amygdala in memory storage: Interaction with other brain systems. Proc. natn. Acad. Sci. U.S.A. 93:1996;13508-13514.
27. McNaughton B. L., Barnes C. A., Meltzer J., Sutherland R. J. Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge. Expl Brain Res. 76:1989;485-496.
28. McNeill T. H., Masters J. N., Finch C. E. Effect of chronic adrenalectomy on neuron loss and distribution of sulfated glycoprotein-2 in the dentate gyrus of prepuberal rats. Expl Neurol. 111:1991;140-144.
29. Micheau J., Destrade C., Soumireu-Mourat B. Time-dependent effects of post-training intrahippocampal injections of corticosterone in retention of appetitive learning tasks in mice. Eur. J. Pharmac. 106:1985;39-46.
30. Mogenson G. J., Yang C. R. The contribution of basal forebrain to limbic-motor integration and the mediation of motivation to action. Adv. exp. med. Biol. 295:1991;267-290.
31. Mondadori C., Weiskrantz L. NMDA receptor blockers facilitate and impair learning via different mechanisms. Behav. neural Biol. 60:1993;205-210.
32. Moser E., Moser M.-B., Andersen P. Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J. Neurosci. 13:1993;3916-3925.
33. Mulder A. B., Lopes da Silva F. H. Interaction of the hippocampus and the basolateral amygdala inputs to the nucleus accumbens of the rat. Soc. Neurosci. Abstr. 22:1996;911.
34. Oitzl M. S., de Kloet E. R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 106:1992;62-71.
35. Packard M. G., Cahill L., McGaugh J. L. Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc. natn. Acad. Sci. U.S.A. 91:1994;8477-8481.
36. Parent M. B., McGaugh J. L. Posttraining infusion of lidocaine into the amygdala basolateral complex impairs retention of inhibitory avoidance training. Brain Res. 661:1994;97-103.
37. Pavlides C., Watanabe Y., McEwen B. S. Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus. 3:1993;183-192.
38. Pavlides C., Kimura A., Magarinos A. M., McEwen B. S. Type-I adrenal steroid receptors prolong hippocampal long-term potentiation. NeuroReport. 5:1994;2673-2677.
39. Paxinos G. and Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, Australia.
40. Quirarte G. L., Roozendaal B., McGaugh J. L. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc. natn. Acad. Sci. U.S.A. 94:1997;14048-14053.
41. Racine R. J., Mingram N. W., Hafner S. Long-term potentiation phenomena in the rat limbic forebrain. Brain Res. 260:1983;915-922.
42. Reul J. M. H. M., de Kloet E. R. Two receptor systems for corticosterone in the rat brain: Microdistribution and differential occupation. Endocrinology. 117:1985;2505-2512.
43. Roozendaal B., Bohus B., McGaugh J. L. Dose-dependent suppression of adrenocortical activity with metyrapone: Effects on emotion and memory. Psychoneuroendocrinology. 21:1996;681-693.
44. Roozendaal B., Cools A. R. Influence of the noradrenergic state of the nucleus accumbens in basolateral amygdala mediated changes in neophobia of rats. Behav. Neurosci. 108:1994;1107-1118.
45. Roozendaal B., McGaugh J. L. Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol. Learn. Memory. 65:1996;1-8.
46. Roozendaal B., McGaugh J. L. The memory-modulatory effects of glucocorticoids depend on an intact stria terminalis. Brain Res. 709:1996;243-250.
47. Roozendaal B., McGaugh J. L. Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage. Neurobiol. Learn. Memory. 67:1997;176-179.
48. Roozendaal B., McGaugh J. L. Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. Eur. J. Neurosci. 9:1997;76-83.
49. Roozendaal B., Portillo-Marquez G., McGaugh J. L. Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. Behav. Neurosci. 110:1996;1074-1083.
50. Roy E. J., Lynn D. M., Bemm C. W. Individual variations in hippocampal dentate degeneration following adrenalectomy. Behav. neural Biol. 54:1990;330-336.
51. Sandi C., Rose S. P. R. Corticosterone enhances long-term potentation in one day-old chicks trained in a weak passive avoidance learning paradigm. Brain Res. 647:1994;106-112.
52. Sapolsky R. M., Stein-Behrens B. A., Armanini M. P. Long-term adrenalectomy causes loss of dentate gyrus and pyramidal neurons in the adult hippocampus. Expl Neurol. 114:1991;246-249.
53. Sloviter R. S., Sollas A. L., Dean E., Neubort S. Adrenalectomy-induced granule cell degeneration in the rat hippocampal dentate gyrus: Characterization of an in vivo model of controlled neuronal death. J. comp. Neurol. 330:1993;324-336.
54. Sloviter R. S., Dean E., Neubort S. Electron microscopic analysis of adrenalectomy-induced hippocampal granule cell degeneration in the rat: Apoptosis in the adult central nervous system. J. comp. Neurol. 330:1993;337-351.
55. Sloviter R. S., Sollas A., Neubort S. Hippocampal dentate granule cell degeneration after adrenalectomy in the rat is not reversed by dexamethasone. Brain Res. 682:1995;227-230.
56. Sloviter R. S., Valiquette G., Abrams G. M., Ronk E. C., Sollas A. L., Paul L. A., Neubort S. Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science. 243:1989;535-538.
57. Sutherland R. J., McDonald R. J. Hippocampus, amygdala and memory deficits in rats. Behav. Brain Res. 37:1990;57-79.
58. Thomas S. R., Assaf S. Y., Iversen S. D. Amygdaloid complex modulates neurotransmission from the entorhinal cortex to the dentate gyrus of the rat. Brain Res. 307:1984;363-365.
59. Tilson H. A., Rogers B. C., Grimes L., Harry G. J., Peterson N. J., Hong J. S., Dyer R. S. Time-dependent neurobiological effects of colchicine administration directly into the hippocampus of rats. Brain Res. 408:1987;163-172.
60. Tomaz C., Dickinson-Anson H., McGaugh J. L. Basolateral amygdala lesions block the diazepam-induced anterograde amnesia in an inhibitory avoidance task. Proc. natn. Acad. Sci. U.S.A. 89:1992;3615-3619.
61. Vaher P. R., Luine V. N., Gould E., McEwen B. S. Effects of adrenalectomy on spatial memory performance and dentate gyrus morphology. Brain Res. 656:1994;71-78.
62. Woolley C. S., Gould E., Sakai R. R., Spencer R. L., McEwen B. S. Effects of aldosterone or RU28362 treatment on adrenalectomy-induced cell death in the dentate gyrus of the adult rat. Brain Res. 554:1991;312-315.